Host–Symbiont–Pathogen–Host Interactions: Wolbachia, Vector-Transmitted Human Pathogens, and the Importance of Quantitative Models of Multipartite Coevolution

Abstract

Infectious disease has been recognized for a long time as an important evolutionary force: It created the need for and shaped the evolution of immune systems and influenced reproduction as well as behavior of many host species. Infectious agents themselves also evolve and must have adapted to host strategies to evade infection, to multiple external and internal environments, and to transmission between hosts. Given the pressure to evolve on both sides, coevolution is expected. Evolution is indeed observed when looking at either host, pathogen, or at other microorganisms directly or indirectly involved and is dependent to some degree on all species interacting. Vector-transmitted diseases with high burden to humans such as malaria and dengue fever are some of many examples where parasites evade the immune system of both mosquito and human hosts, thereby maximizing the vector’s transmission and persistence. Arthropod hosts such as mosquitos may also be carriers of vertically transmitted endosymbionts, such as the Wolbachia bacterium, that also induce a complex modification of the arthropod’s life history traits. This sort of scenario illustrates the need to consider ecological, multipartite, and evolutionary models—the relevance to human health, together with extensive data collection from epidemiological surveillance, provides an opportunity to expand and improve evolutionary theory.

Glossary

Artificial selection

Consists of creating conditions (usually in a laboratory setting) that favor certain variants provided they exist in the previous populations—to be more represented in the following generations, e.g., infecting flies with a virulent pathogen will cause resistant flies to increase in frequency. Artificial selection is useful for detecting and quantifying variation for certain traits

Bayesian statistics

One of the two main statistical philosophies, as opposed to frequentist statistics, based on the original work of Bayes, requires using (or assuming to the best of knowledge lack of) prior knowledge as input and dealing with uncertainty in the parameter estimates

Cross-protection or cross-enhancement

Phenomenon by which infection with a pathogen (or serotype) either makes a secondary infection less (protection) or more (enhancement) likely

Deterministic models

Models that do not take chance events into account and approximate the occurrence of events by the average or expected rate

Disease ecology

The study of disease as species that colonize niches (usually hosts, but also intermediate environmental stages or secondary hosts)

Endemic transmission

Continual transmission of disease, which may still vary for reasons such as seasons or immunization, but does not depend on external introduction of the pathogen

Evolutionary stable (strategy)

An ESS is a trait value or a combination of values that cannot be beaten by any other, and therefore, once achieved, it stays the same in the population (provided the environment does not change). If more than one organism is evolving in response to the others, a coevolutionary stable strategy, CSS, can be achieved, so that individuals of any species with different trait values cannot succeed in the population better than the ones that have achieved it

F_IS, F_ST

Measures of genetic differentiation. F_IS is the inbreeding coefficient, which is a measure of consanguinity, or relationship. F_ST is a measure of variation within a subpopulation compared to the variation in the total population

Fitness

The capacity of an individual or population to propagate and persist in the population fitness has many components such as fecundity (the more offspring a variant has, the more successful it will be), survival (the better it survives, the more it will be present), and many others

Genetic background

The genetic sequence of an individual. Clones of a laboratory animal share a same genetic background

Heritable genetic variation

The distribution in a population of variants of any genes, i.e., variants that can be transmitted genetically from parent to offspring

Incidence (of disease)

The number of new infections in a given time period, e.g., the weekly incidence of dengue fever is the number of new cases of the disease in a particular week (also usually defined for a geographic region, like a city)

Least-squares fitting

Frequentist estimation method that minimizes the square of the distance between the data points and a curve (straight line, function, or model) and should explain the trends observed

Neutral evolution

Evolution that does not depend on natural selection, most readily exemplified by sequence variation that has no function and therefore does not affect survival, i.e., is neutral

Phenotypic evolution

Evolution of observable traits, usually equated to evolution of traits under selection

Phenotypic variation

Distribution of trait values, e.g., height in a human population

Polymorphism

Variation. A polymorphic gene is a gene that differs in individuals (or the pair of chromosomes of a single individual)

Prevalence (of disease)

The number of disease cases in a certain point in time

Priming (Immune system)

Upregulating immune responses that would then respond more readily to an aggression, e.g., exposing the immune system to a bacterium may activate responses that would then help kill viruses introduced afterwards

Random genetic drift

Process by which, due to chance in reproduction, some individuals pass on offspring (and therefore genes) to the next generation, while others do not. As a consequence, over some time, there is a finite probability that some genes get lost and others get fixed without there being any selection for them. In Motoo Kimura’s words, it is the “survival of the luckiest”

Reciprocal interactions, Feedback

Any mechanism that allows a process to self-regulate or self-enhance is termed feedback; ecology affects evolution, and in the case where evolution of traits affects ecology in the short term, it is said that the relationship between ecology and evolution is reciprocal

Selection coefficient

The mathematical representation of selection, usually as a single parameter (s)

Selection, selective pressure

Any process that favors specific variants in the population, e.g., pesticides favor the survival of resistant pests, and therefore selects them for future generations

Serotype

Pathogen type that elicits a specific immune response and therefore is distinguished from similar pathogens based on its antigens and matching antibodies produced against them

Statistical inference, fitting

Any method that adjusts free parameters of a curve (function or model) to find the values that best explain the observed data, i.e., that best “fits” the data

Sylvatic transmission cycle

Disease transmission that happens among wild animals, independently from humans

Temporary cross-immunity

Temporary cross-protection that wanes after some time

Theoretical epidemiology

Broadly similar to disease ecology, but associated more with the theoretical aspects of the practice of epidemiology, as opposed to the study of diversity of pathogens